FACTORIAL ANALYSIS OF ZINC SERUM LEVELS, FATTY ACIDS, OXIDATIVE STRESS PARAMETERS AND SUPPLEMENTATION ON ASSISTED REPRODUCTIVE TECHNOLOGY OUTCOME
Keywords:
Keywords: assisted reproduction, fatty acids, oxidative stress, zinc
Abstract
Background: Infertility remains a prevalent global reproductive challenge significantly affecting the lives of couples worldwide. The etiology of infertility can be affected by various factors that exhibit possible relationships with one another’s. The aim of the study was to investigate factors that can interact and influence the pregnancy outcome in couples undergoing assisted reproductive technology procedure.
Methods: This retrospective study included 64 couples (64 men and their female partners) undergoing assisted reproductive technology procedure, having different pregnancy outcomes and lifestyle habits. Biomarkers of antioxidative and fatty acids status in serum of both male and female partners, as well as the concentration of Zinc in serum and seminal plasma of men; and their impact on assisted reproductive technology outcome were examined.
Results: We grouped the parameters using principal component analysis and identified the three most contributing factors to the pregnancy achievement – seminogram parameters in males and redox status scores in female participants; supplementation with vitamin D, magnesium, and zinc; and serum levels of omega-3 and omega-6 fatty acids.
Conclusion: The study concluded that seminogram parameters, intake of micronutrients and levels of Zinc and omega-3 and omega-6 fatty acids are contributing factors to assisted reproductive technology success. Further studies on a larger cohort are needed to confirm the predictive role of these factors on the success of assisted reproductive technology.
References
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2. Chen X, Ren C, Wu C, Liu X. Mendelian randomization reveals the impact of diet on infertility in men and women. Front Endocrinol (Lausanne). 2024;15:1376800.
3. Graham ME, Jelin A, Hoon Jr AH, Wilms Floet AM, Levey E, Graham EM. Assisted reproductive technology: Short‐and long‐term outcomes. Dev Med Child Neurol. 2023;65(1):38-49.
4. Foucaut A-M, Faure C, Julia C, Czernichow S, Levy R, Dupont C, et al. Sedentary behavior, physical inactivity and body composition in relation to idiopathic infertility among men and women. PLoS One. 2019;14(4):e0210770.
5. Chao H-H, Zhang Y, Dong P-Y, Gurunathan S, Zhang X-F. Comprehensive review on the positive and negative effects of various important regulators on male spermatogenesis and fertility. Frontiers in Nutrition. 2023;9:1063510.
6. Allouche-Fitoussi D, Breitbart H. The role of zinc in male fertility. International journal of molecular sciences. 2020;21(20):7796.
7. Olechnowicz J, Tinkov A, Skalny A, Suliburska J. Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. The journal of physiological sciences. 2018;68(1):19-31.
8. Kotur-Stevuljević J, Savić J, Simić M, Ivanišević J. Redox homeostasis, oxidative stress and antioxidant system in health and disease: the possibility of modulation by antioxidants. Arhiv za farmaciju. 2023;73(4):251-63.
9. Chasapis CT, Ntoupa P-SA, Spiliopoulou CA, Stefanidou ME. Recent aspects of the effects of zinc on human health. Arch Toxicol. 2020;94:1443-60.
10. Santos HO, Teixeira FJ, Schoenfeld BJ. Dietary vs. pharmacological doses of zinc: A clinical review. Clin Nutr. 2020;39(5):1345-53.
11. Nenkova G, Petrov L, Alexandrova A. Role of trace elements for oxidative status and quality of human sperm. Balkan medical journal. 2017;34(4):343-8.
12. Harchegani AB, Dahan H, Tahmasbpour E, Shahriary A. Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis. Human Fertility. 2018.
13. Becatti M, Fucci R, Mannucci A, Barygina V, Mugnaini M, Criscuoli L, et al. A biochemical approach to detect oxidative stress in infertile women undergoing assisted reproductive technology procedures. International journal of molecular sciences. 2018;19(2):592.
14. Eskew AM, Wormer KC, Matthews ML, Norton HJ, Papadakis MA, Hurst BS. The association between fatty acid index and in vitro fertilization outcomes. J Assist Reprod Genet. 2017;34:1627-32.
15. Stanhiser J, Jukic AMZ, Steiner AZ. Serum omega-3 and omega-6 fatty acid concentrations and natural fertility. Hum Reprod. 2020;35(4):950-7.
16. Collodel G, Moretti E, Noto D, Iacoponi F, Signorini C. Fatty acid profile and metabolism are related to human sperm parameters and are relevant in idiopathic infertility and varicocele. Mediators Inflamm. 2020;2020.
17. Safarinejad MR, Hosseini SY, Dadkhah F, Asgari MA. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin Nutr. 2010;29(1):100-5.
18. World Health O. WHO laboratory manual for the examination and processing of human semen. 5th ed ed. Geneva: World Health Organization; 2010.
19. Garalejic E, Arsic B, Radakovic J, Bojovic Jovic D, Lekic D, Macanovic B, et al. A preliminary evaluation of influence of body mass index on in vitro fertilization outcome in non-obese endometriosis patients. BMC Womens Health. 2017;17:1-9.
20. Perovic MD, Sudar-Milovanovic EM, Simonovic ED, Resanovic IM, Draganic VD, Radakovic JD, et al. Hypothesis regarding the effects of gonadotropins on the level of free fatty acids and phospholipids in serum and follicular fluid during controlled ovarian stimulation. Med Hypotheses. 2019;123:30-4.
21. Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49(5):1304-13.
22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
23. Alamdari DH, Paletas K, Pegiou T, Sarigianni M, Befani C, Koliakos G. A novel assay for the evaluation of the prooxidant–antioxidant balance, before and after antioxidant vitamin administration in type II diabetes patients. Clin Biochem. 2007;40(3-4):248-54.
24. Paunovic M, Kotur-Stevuljevic J, Arsic A, Milosevic M, Todorovic V, Guzonjic A, et al. Antioxidative Effects of Black Currant and Cornelian Cherry Juices in Different Tissues of an Experimental Model of Metabolic Syndrome in Rats. Antioxidants. 2023;12(6):1148.
25. Pipingas A, Cockerell R, Grima N, Sinclair A, Stough C, Scholey A, et al. Randomized controlled trial examining the effects of fish oil and multivitamin supplementation on the incorporation of n-3 and n-6 fatty acids into red blood cells. Nutrients. 2014;6(5):1956-70.
26. Bar–Or D, Lau E, Winkler JV. A novel assay for cobalt-albumin binding and its potential as a marker for myocardial ischemia—a preliminary report. The Journal of emergency medicine. 2000;19(4):311-5.
27. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82(1):70-7.
28. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85.
29. Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170-5.
30. Kotur-Stevuljevic J, Bogavac-Stanojevic N, Jelic-Ivanovic Z, Stefanovic A, Gojkovic T, Joksic J, et al. Oxidative stress and paraoxonase 1 status in acute ischemic stroke patients. Atherosclerosis. 2015;241(1):192-8.
31. Thorlaksdottir A, Skuladottir G, Petursdottir A, Tryggvadottir L, Ogmundsdottir H, Eyfjord J, et al. Positive association between plasma antioxidant capacity and n− 3 PUFA in red blood cells from women. Lipids. 2006;41:119-25.
32. Quintana-Villamandos B, Pazó-Sayós L, González del Pozo I, Rodríguez-Rodríguez P, Bellón JM, Pedraz-Prieto Á, et al. OXY-SCORE: a new perspective for left ventricular hypertrophy diagnosis. Ther Adv Chronic Dis. 2020;11:2040622320936417.
33. Arsic A, Krstic P, Paunovic M, Nedovic J, Jakovljevic V, Vucic V. Anti-inflammatory effect of combining fish oil and evening primrose oil supplementation on breast cancer patients undergoing chemotherapy: a randomized placebo-controlled trial. Sci Rep. 2023;13(1):6449.
34. Popovic T, Ranic M, Bulajic P, Milicevic M, Arsic A, Vucic V, et al. Effects of n-3 fatty acids supplementation on plasma phospholipids fatty acid composition in patients with obstructive jaundice-a pilot study. J Clin Biochem Nutr. 2009;45(3):370-5.
35. Wong WY, Flik G, Groenen PM, Swinkels DW, Thomas CM, Copius-Peereboom JH, et al. The impact of calcium, magnesium, zinc, and copper in blood and seminal plasma on semen parameters in men. Reprod Toxicol. 2001;15(2):131-6.
36. Tulić L. Oksidativni stres i ravnoteža bioelemenata kod pacijentkinja u postupku vantelesnog oplođenja. Универзитет у Београду. 2019.
37. Aydin Y, Ozatik O, Hassa H, Ulusoy D, Ogut S, Sahin F. Relationship between oxidative stress and clinical pregnancy in assisted reproductive technology treatment cycles. J Assist Reprod Genet. 2013;30:765-72.
38. Verit FF, Verit A, Ciftci H, Erel O, Celik H. Paraoxonase‐1 activity in subfertile men and relationship to sperm parameters. J Androl. 2009;30(2):183-9.
39. Beyazıt F, Balcı O, Adam M, İnal H, Bardakcı Y, Yılmaz N. Serum ischemia modified albumin levels in infertile couples underwent in vitro fertilization. Gynecology Obstetrics & Reproductive Medicine. 2015;21(1):14-7.
40. Todorović MB, Čabarkapa VS, Đerić MJ, Suđi JЈ, Ilinčić BP, Trifu AD, et al. Zinc status in adults in northern Serbia. Food and Feed research. 2019;46(1):99-110.
41. Tulić L, Ćurčić M, Stojnić J, Bulat Z, Protić I. Correlation of oxidative stress markers and semen parameters with the outcome of in vitro fertilization. Srp Arh Celok Lek. 2020;148(5-6):310-4.
42. Özkaya MO, Nazıroğlu M. Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilization. Fertil Steril. 2010;94(6):2465-6.
43. Niramitmahapanya S, Harris SS, Dawson-Hughes B. Type of dietary fat is associated with the 25-hydroxyvitamin D3 increment in response to vitamin D supplementation. The Journal of Clinical Endocrinology & Metabolism. 2011;96(10):3170-4.
44. Uwitonze AM, Razzaque MS. Role of magnesium in vitamin D activation and function. Journal of Osteopathic Medicine. 2018;118(3):181-9.
45. Monteiro JP, Fuzo CA, Ued FV, Kaput J. Dietary patterns related to zinc and polyunsaturated fatty acids intake are associated with serum linoleic/dihomo-γ-linolenic ratio in NHANES males and females. Sci Rep. 2021;11(1):12215.
46. Knez M, Pantovic A, Zekovic M, Pavlovic Z, Glibetic M, Zec M. Is there a link between zinc intake and status with plasma fatty acid profile and desaturase activities in dyslipidemic subjects? Nutrients. 2019;12(1):93.
47. Hernández MC, Rojas P, Carrasco F, Basfi-Fer K, Valenzuela R, Codoceo J, et al. Fatty acid desaturation in red blood cell membranes of patients with type 2 diabetes is improved by zinc supplementation. J Trace Elem Med Biol. 2020;62:126571.
48. Dai P, Zou M, Cai Z, Zeng X, Zhang X, Liang M. pH Homeodynamics and Male Fertility: A Coordinated Regulation of Acid-Based Balance during Sperm Journey to Fertilization. Biomolecules. 2024;14(6):685.
49. Zhou J, Chen L, Li J, Li H, Hong Z, Xie M, et al. The semen pH affects sperm motility and capacitation. PLoS One. 2015;10(7):e0132974.
50. Su Z, Ding P, Su W, Li X, Li Y, Li X, et al. Association between oxidative balance score and female infertility from the national health and nutrition examination survey 2013–2018. Front Endocrinol (Lausanne). 2024;15:1386021.
51. Luddi A, Capaldo A, Focarelli R, Gori M, Morgante G, Piomboni P, et al. Antioxidants reduce oxidative stress in follicular fluid of aged women undergoing IVF. Reprod Biol Endocrinol. 2016;14:1-7.
52. Schaefer E, Nock D. The impact of preconceptional multiple-micronutrient supplementation on female fertility. Clinical Medicine Insights: Women's Health. 2019;12:1179562X19843868.
53. Abodi M, De Cosmi V, Parazzini F, Agostoni C. Omega-3 fatty acids dietary intake for oocyte quality in women undergoing assisted reproductive techniques: A systematic review. European journal of obstetrics & gynecology and reproductive biology. 2022;275:97-105.
2. Chen X, Ren C, Wu C, Liu X. Mendelian randomization reveals the impact of diet on infertility in men and women. Front Endocrinol (Lausanne). 2024;15:1376800.
3. Graham ME, Jelin A, Hoon Jr AH, Wilms Floet AM, Levey E, Graham EM. Assisted reproductive technology: Short‐and long‐term outcomes. Dev Med Child Neurol. 2023;65(1):38-49.
4. Foucaut A-M, Faure C, Julia C, Czernichow S, Levy R, Dupont C, et al. Sedentary behavior, physical inactivity and body composition in relation to idiopathic infertility among men and women. PLoS One. 2019;14(4):e0210770.
5. Chao H-H, Zhang Y, Dong P-Y, Gurunathan S, Zhang X-F. Comprehensive review on the positive and negative effects of various important regulators on male spermatogenesis and fertility. Frontiers in Nutrition. 2023;9:1063510.
6. Allouche-Fitoussi D, Breitbart H. The role of zinc in male fertility. International journal of molecular sciences. 2020;21(20):7796.
7. Olechnowicz J, Tinkov A, Skalny A, Suliburska J. Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. The journal of physiological sciences. 2018;68(1):19-31.
8. Kotur-Stevuljević J, Savić J, Simić M, Ivanišević J. Redox homeostasis, oxidative stress and antioxidant system in health and disease: the possibility of modulation by antioxidants. Arhiv za farmaciju. 2023;73(4):251-63.
9. Chasapis CT, Ntoupa P-SA, Spiliopoulou CA, Stefanidou ME. Recent aspects of the effects of zinc on human health. Arch Toxicol. 2020;94:1443-60.
10. Santos HO, Teixeira FJ, Schoenfeld BJ. Dietary vs. pharmacological doses of zinc: A clinical review. Clin Nutr. 2020;39(5):1345-53.
11. Nenkova G, Petrov L, Alexandrova A. Role of trace elements for oxidative status and quality of human sperm. Balkan medical journal. 2017;34(4):343-8.
12. Harchegani AB, Dahan H, Tahmasbpour E, Shahriary A. Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis. Human Fertility. 2018.
13. Becatti M, Fucci R, Mannucci A, Barygina V, Mugnaini M, Criscuoli L, et al. A biochemical approach to detect oxidative stress in infertile women undergoing assisted reproductive technology procedures. International journal of molecular sciences. 2018;19(2):592.
14. Eskew AM, Wormer KC, Matthews ML, Norton HJ, Papadakis MA, Hurst BS. The association between fatty acid index and in vitro fertilization outcomes. J Assist Reprod Genet. 2017;34:1627-32.
15. Stanhiser J, Jukic AMZ, Steiner AZ. Serum omega-3 and omega-6 fatty acid concentrations and natural fertility. Hum Reprod. 2020;35(4):950-7.
16. Collodel G, Moretti E, Noto D, Iacoponi F, Signorini C. Fatty acid profile and metabolism are related to human sperm parameters and are relevant in idiopathic infertility and varicocele. Mediators Inflamm. 2020;2020.
17. Safarinejad MR, Hosseini SY, Dadkhah F, Asgari MA. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin Nutr. 2010;29(1):100-5.
18. World Health O. WHO laboratory manual for the examination and processing of human semen. 5th ed ed. Geneva: World Health Organization; 2010.
19. Garalejic E, Arsic B, Radakovic J, Bojovic Jovic D, Lekic D, Macanovic B, et al. A preliminary evaluation of influence of body mass index on in vitro fertilization outcome in non-obese endometriosis patients. BMC Womens Health. 2017;17:1-9.
20. Perovic MD, Sudar-Milovanovic EM, Simonovic ED, Resanovic IM, Draganic VD, Radakovic JD, et al. Hypothesis regarding the effects of gonadotropins on the level of free fatty acids and phospholipids in serum and follicular fluid during controlled ovarian stimulation. Med Hypotheses. 2019;123:30-4.
21. Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, et al. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49(5):1304-13.
22. Erel O. A new automated colorimetric method for measuring total oxidant status. Clin Biochem. 2005;38(12):1103-11.
23. Alamdari DH, Paletas K, Pegiou T, Sarigianni M, Befani C, Koliakos G. A novel assay for the evaluation of the prooxidant–antioxidant balance, before and after antioxidant vitamin administration in type II diabetes patients. Clin Biochem. 2007;40(3-4):248-54.
24. Paunovic M, Kotur-Stevuljevic J, Arsic A, Milosevic M, Todorovic V, Guzonjic A, et al. Antioxidative Effects of Black Currant and Cornelian Cherry Juices in Different Tissues of an Experimental Model of Metabolic Syndrome in Rats. Antioxidants. 2023;12(6):1148.
25. Pipingas A, Cockerell R, Grima N, Sinclair A, Stough C, Scholey A, et al. Randomized controlled trial examining the effects of fish oil and multivitamin supplementation on the incorporation of n-3 and n-6 fatty acids into red blood cells. Nutrients. 2014;6(5):1956-70.
26. Bar–Or D, Lau E, Winkler JV. A novel assay for cobalt-albumin binding and its potential as a marker for myocardial ischemia—a preliminary report. The Journal of emergency medicine. 2000;19(4):311-5.
27. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82(1):70-7.
28. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem. 2004;37(4):277-85.
29. Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170-5.
30. Kotur-Stevuljevic J, Bogavac-Stanojevic N, Jelic-Ivanovic Z, Stefanovic A, Gojkovic T, Joksic J, et al. Oxidative stress and paraoxonase 1 status in acute ischemic stroke patients. Atherosclerosis. 2015;241(1):192-8.
31. Thorlaksdottir A, Skuladottir G, Petursdottir A, Tryggvadottir L, Ogmundsdottir H, Eyfjord J, et al. Positive association between plasma antioxidant capacity and n− 3 PUFA in red blood cells from women. Lipids. 2006;41:119-25.
32. Quintana-Villamandos B, Pazó-Sayós L, González del Pozo I, Rodríguez-Rodríguez P, Bellón JM, Pedraz-Prieto Á, et al. OXY-SCORE: a new perspective for left ventricular hypertrophy diagnosis. Ther Adv Chronic Dis. 2020;11:2040622320936417.
33. Arsic A, Krstic P, Paunovic M, Nedovic J, Jakovljevic V, Vucic V. Anti-inflammatory effect of combining fish oil and evening primrose oil supplementation on breast cancer patients undergoing chemotherapy: a randomized placebo-controlled trial. Sci Rep. 2023;13(1):6449.
34. Popovic T, Ranic M, Bulajic P, Milicevic M, Arsic A, Vucic V, et al. Effects of n-3 fatty acids supplementation on plasma phospholipids fatty acid composition in patients with obstructive jaundice-a pilot study. J Clin Biochem Nutr. 2009;45(3):370-5.
35. Wong WY, Flik G, Groenen PM, Swinkels DW, Thomas CM, Copius-Peereboom JH, et al. The impact of calcium, magnesium, zinc, and copper in blood and seminal plasma on semen parameters in men. Reprod Toxicol. 2001;15(2):131-6.
36. Tulić L. Oksidativni stres i ravnoteža bioelemenata kod pacijentkinja u postupku vantelesnog oplođenja. Универзитет у Београду. 2019.
37. Aydin Y, Ozatik O, Hassa H, Ulusoy D, Ogut S, Sahin F. Relationship between oxidative stress and clinical pregnancy in assisted reproductive technology treatment cycles. J Assist Reprod Genet. 2013;30:765-72.
38. Verit FF, Verit A, Ciftci H, Erel O, Celik H. Paraoxonase‐1 activity in subfertile men and relationship to sperm parameters. J Androl. 2009;30(2):183-9.
39. Beyazıt F, Balcı O, Adam M, İnal H, Bardakcı Y, Yılmaz N. Serum ischemia modified albumin levels in infertile couples underwent in vitro fertilization. Gynecology Obstetrics & Reproductive Medicine. 2015;21(1):14-7.
40. Todorović MB, Čabarkapa VS, Đerić MJ, Suđi JЈ, Ilinčić BP, Trifu AD, et al. Zinc status in adults in northern Serbia. Food and Feed research. 2019;46(1):99-110.
41. Tulić L, Ćurčić M, Stojnić J, Bulat Z, Protić I. Correlation of oxidative stress markers and semen parameters with the outcome of in vitro fertilization. Srp Arh Celok Lek. 2020;148(5-6):310-4.
42. Özkaya MO, Nazıroğlu M. Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilization. Fertil Steril. 2010;94(6):2465-6.
43. Niramitmahapanya S, Harris SS, Dawson-Hughes B. Type of dietary fat is associated with the 25-hydroxyvitamin D3 increment in response to vitamin D supplementation. The Journal of Clinical Endocrinology & Metabolism. 2011;96(10):3170-4.
44. Uwitonze AM, Razzaque MS. Role of magnesium in vitamin D activation and function. Journal of Osteopathic Medicine. 2018;118(3):181-9.
45. Monteiro JP, Fuzo CA, Ued FV, Kaput J. Dietary patterns related to zinc and polyunsaturated fatty acids intake are associated with serum linoleic/dihomo-γ-linolenic ratio in NHANES males and females. Sci Rep. 2021;11(1):12215.
46. Knez M, Pantovic A, Zekovic M, Pavlovic Z, Glibetic M, Zec M. Is there a link between zinc intake and status with plasma fatty acid profile and desaturase activities in dyslipidemic subjects? Nutrients. 2019;12(1):93.
47. Hernández MC, Rojas P, Carrasco F, Basfi-Fer K, Valenzuela R, Codoceo J, et al. Fatty acid desaturation in red blood cell membranes of patients with type 2 diabetes is improved by zinc supplementation. J Trace Elem Med Biol. 2020;62:126571.
48. Dai P, Zou M, Cai Z, Zeng X, Zhang X, Liang M. pH Homeodynamics and Male Fertility: A Coordinated Regulation of Acid-Based Balance during Sperm Journey to Fertilization. Biomolecules. 2024;14(6):685.
49. Zhou J, Chen L, Li J, Li H, Hong Z, Xie M, et al. The semen pH affects sperm motility and capacitation. PLoS One. 2015;10(7):e0132974.
50. Su Z, Ding P, Su W, Li X, Li Y, Li X, et al. Association between oxidative balance score and female infertility from the national health and nutrition examination survey 2013–2018. Front Endocrinol (Lausanne). 2024;15:1386021.
51. Luddi A, Capaldo A, Focarelli R, Gori M, Morgante G, Piomboni P, et al. Antioxidants reduce oxidative stress in follicular fluid of aged women undergoing IVF. Reprod Biol Endocrinol. 2016;14:1-7.
52. Schaefer E, Nock D. The impact of preconceptional multiple-micronutrient supplementation on female fertility. Clinical Medicine Insights: Women's Health. 2019;12:1179562X19843868.
53. Abodi M, De Cosmi V, Parazzini F, Agostoni C. Omega-3 fatty acids dietary intake for oocyte quality in women undergoing assisted reproductive techniques: A systematic review. European journal of obstetrics & gynecology and reproductive biology. 2022;275:97-105.
Published
2025/03/23
Section
Original paper
Copyright (c) 2025 Aleksandra Veselinovic
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